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417PALEOBIOGEOGRAPHY AND TAXONOMY GENUS CONCHOLEPASRevista Chilena de Historia Natural81: 417-436, 2008

Paleobiogeography and taxonomy of the genus Concholepas(Lamarck, 1801): a review and new evidences

Paleobiogeografía y taxonomía del género Concholepas (Lamarck, 1801):una revisión y nuevas evidencias

LEYLA CÁRDENAS1, 3, *, FRÉDÉRIQUE VIARD2 & JUAN CARLOS CASTILLA1

1 Center for Advanced Studies in Ecology and Biodiversity (CASEB), Facultad de Ciencias Biológicas,Pontificia Universidad Católica de Chile, Chile

2 Equipe Evolution et Génétique des Populations Marines, LIA “DIAMS”, UMR 7144 CNRS-Université Pierre etMarie Curie, Station Biologique Roscoff, France

3 Instituto de Ecología y Evolución, Universidad Austral de Chile, Campus Isla Teja, Casilla 567, Valdivia, Chile*e-mail for correspondence: [email protected]

ABSTRACT

The muricid gastropod Concholepas concholepas, known in Chile as ‘loco’, is an important component ofintertidal and shallow subtidal communities, and is one of the main invertebrates targeted by small-scalefishers (divers) in Chile. Because of its ecological importance and economical value, numerous studies havebeen conducted to describe its life history, ecology and to understand population dynamics, fishery andmanagement. However, little effort has been done to address the causal factor (s) behind its currentgeographic distribution and moreover little is known about the past distribution of the different species in thegenus. In this paper, first we review the paleobiogeography, historical relationships, taxonomy andgeographical distribution of Concholepas species, so to contribute in the reconstruction on the past history ofthe genus. Second, we discuss the robustness of using shell traits when classifying specimens of the genusConcholepas. Third, we evaluate the taxonomic status of C. concholepas including samples from Peru, thecontinental coast of Chile and Juan Fernández Archipelago, using a molecular approach. Four mainconclusions are reached: (1) the evolutionary history of the genus Concholepas has been characterized bysuccessive phenotypically different forms where the fossils species appear to be distinguishable states in thesame evolving lineage; (2) the historical biogeography of Concholepas was probably the result of a southwarddirection process of expansions and extinctions, with the ancestral species being located in south-central Peru;(3) C. concholepas corresponds to a single taxonomic unit along its continental geographical range ofdistribution; (4) the mtDNA variation present in C. concholepas does not support the existence of thesubspecies C. concholepas fernandizianus in the Juan Fernández Archipelago. We suggest that these resultsshould be considered in future ecological, fishery, management and conservation studies on C. concholepasalong the Peruvian and Chilean coast and in the Juan Fernández Archipelago.

Key words: paleobiogeography, southeastern Pacific coast, Concholepas, fossil record, taxonomy, mtDNAvariation.

RESUMEN

El gastrópodo muricido Concholepas concholepas, conocido en Chile como ‘loco’, es un importantecomponente de comunidades marinas intermareales y submareales y es una de las principales especies deinvertebrados en la pesquería artesanal chilena. Debido a su importancia y valor económico, se han realizadonumerosos estudios para describir su historia de vida, ecología y entender las dinámicas poblacionales,pesquería y manejo. Sin embargo, menores esfuerzos han sido realizados para entender los factores causalesdetrás de su actual distribución geográfica y más aún poco es conocido acerca de la pasada distribución de lasdiferentes especies del género. En este trabajo, nosotros primero revisamos la paleobiogeografía, relacioneshistóricas y taxonomía, de las especies del género Concholepas para contribuir en la reconstrucción de lahistoria pasada del género. Segundo, discutimos la robustez de usar caracteres morfológicos en la taxonomíadel género. Tercero, usando una aproximación molecular evaluamos el estatus taxonómico de C. concholepasincluyendo muestras desde Perú, la costa continental de Chile y del archipiélago de Juan Fernández. Seobtuvieron cuatro conclusiones principales: (1) la historia evolutiva del género Concholepas ha sidocaracterizada por sucesivas formas fenotípicamente diferentes, donde las especies fósiles parecen ser estados

418 CÁRDENAS ET AL.

morfológicos distinguibles de un único linaje evolutivo; (2) la biogeografía histórica de Concholepas pareceser resultado de un proceso continuo de expansión y extinción con dirección sur, con las especies ancestraleslocalizadas en el centro-sur de Perú; (3) C. concholepas corresponde a una sola unidad taxonómica a lo lagode su rango de distribución continental; (4) la variación en el ADNmt detectada en C. concholepas no apoyala existencia de la subespecie C. concholepas fernandizianus en el Archipiélago de Juan Fernández.Sugerimos que estos resultados deberán ser considerados en futuros estudios de ecología, pesquería,conservación y manejo en C. concholepas a lo largo de la costa chileno-peruana y en el archipiélago de JuanFernández.

Palabras clave: paleobiogeografía, costa sur-este del Océano Pacífico, Concholepas, registro fósil,taxonomía, variación en el ADNmt.

INTRODUCTION

The marine gastropod Concholepasconcholepas (Bruguière, 1789), is a benthicspecies endemic of the Southeastern Pacificcoast and the only extant species of the genusConcholepas (Lamarck, 1801). At present, C.concholepas has a distribution ranging fromtropical (Lobos Afuera Island, 6º27’ S, Stuardo1979) to subantartic zones (Cape Horn, 56°00’S, Castilla & Guiñez 2000), showing also apopulation in the Juan Fernández Archipelago(33º36' S), distant 587 km from Chileancontinental coastline. Due to its high economicvalue (Leiva & Castil la 2002) and keyecological role in intertidal and subtidal rockycommunities, this species has been intensivelystudied during the past two decades (Castilla &Durán 1985, Moreno et al. 1986, Durán &Castilla 1989, Power et al. 1996, Castilla 1999,Manríquez & Castilla 2001, Poulin et al.2002a). However, little effort has been done toaddress the causal factor (s) behind its currentgeographic distribution. Given its widedistribution, C. concholepas is included in allsoutheastern Pacific biogeographic zones as aspecies that crosses biogeographical barriers(Broitman et al . 2001). The moderngeographical distribution of C. concholepastogether with its local adaptations is a blendingof historical and contemporary processes. Thus,its geographical distributional range is a resultof a dynamic process through evolutionarytime. At present, along its geographical range,C. concholepas is under the influence ofoceanographic (e.g., Humboldt and Cape Horn)and coastal currents, climatic systems (e.g.,subtropical, temperate, cold) and anthropogenicfactors (Castilla 1999). Moreover, in the pastthe Southeastern Pacific coastal realm hasexperienced major environmental changes, suchas intense oceanographic, climatic and

geomorphologic modifications, which occurredduring the Neogene (Martínez-Pardo 1990),that have shaped the present marinebiogeography scenario (Camus 2001). Mostprobably an important part of the history of C.concholepas may be the result of the greatspatial/temporal environmental variabilityalong its distributional range. Therefore, inorder to understand its current geographicdistribution pattern, a historical approach mustbe considered.

Traditionally, the genus Concholepas wasassigned to the muricid subfamily Thaidinae(Jousseaume, 1888) (Herm 1969, Lambiotte1975, Stuardo 1979). However, according tothe cladistic approach of Kool (1993), thegenus Concholepas should be assigned to theredefined subfamily Rapaninae Gray, 1853.The Rapaninae clade comprises a large groupof Eocene to contemporary predatory marinegastropods, all being prominent members ofsubtropical and tropical shallow-watercommunities (Vermeij & Carlson 2000).Several authors have suggested that theecological specialization and functionaldiversification of the rapanines occurred attimes and places of high species richness andsubstantial ecological complexity, particularlyin the post-Oligocene Indo-west Pacific regionand in the tropical America during the Neogene(Vermeij 1987, Kool 1993, Vermeij & Carlson2000). Apparently, the specialization within thegroup occurred in a period characterized by awider equatorial belt relative to the present one,when rapanines were strongly restricted bycompetition and predators, leading them toinvade coastal refuges including the upperzones of the rocky intertidal (Vermeij 1987).

Studies of past geographical distribution ofConcholepas include considerations of thetaxonomy and phylogenetic relationshipsbetween the species of the genus and have

419PALEOBIOGEOGRAPHY AND TAXONOMY GENUS CONCHOLEPAS

focused on fossil specimens and definition ofspecies based on morphological traits, such asfor instance: the form and position of the spire,shell thickness, body whorl rotation and shelllength/width ratios (Ponder & Lindberg 1997).Although traditionally the gastropodsclassification and phylogeny are based onhardshell structure, morphological variationswithin species are recognized (Currey &Hughes 1982, Janson 1982, Janson 1983,Janson & Ward 1985). This situation oftentranslates into serious difficulties regardingspecies identification, lack of confidence insystematic conclusions, generally poorlyresolved phylogenetic hypotheses and unstabletaxonomies (Schander & Sundberg 2001, Collin2003a). Hence, molecular markers have beenconsidered as useful tools to evaluate whethermorphological variations corresponds to theexpression of differences related to thepresence of two or more species or related tophenotypic expressions linked to environmentalvariation (Via & Lande 1985, Stearns 1989,Johanesson & Johanesson 1990, Johanesson etal. 1993, Scheiner 1993, Dalby 1997, Soler etal. 2000).

The genus Concholepas is mainly the resultof extinct species, and therefore, an evaluationof its the taxonomy appears difficult. Forexample, for some Concholepas fossils therepresentation of specimens is extremely low(DeVries 2000). Collecting additional materialmay be prohibitive because of the rarity of thefossils, inaccessibili ty of the habitat ordestruction of known collection localities.Besides, many of the fossil specimens availableare incomplete or represented by fragmentedshells and have been deposited in differentmuseums around the world. In the past years,several taxonomical modifications on extantand fossil Concholepas species have beensuggested, including the description of newspecies, subspecies and modifications ongeographical distributions (Stuardo 1979,Kensley 1985, Vermeij 1998, DeVries 1995,2000). Also, authors have proposed a differenttaxonomic status among extant populations ofC. concholepas, based on characteristics of theshell, the shape of the foot and differences inthe lateral teeth. For instance, taking intoaccount the shell morphology andornamentation among different C. concholepascontinental populations and those from the Juan

Fernández Archipelago, Stuardo (1979)suggested the existence a subspecies in theArchipelago: C. concholepas fernandezianus.In this case, to understand biogeographicprocesses and patterns of speciation on C.concholepas would require evaluating whenand how this species arrived to theArchipelago, and to follow the degree ofdiversification.

Attempts have been made in the coast ofChile and Perú to analyze genetic differencesamong C. concholepas populations. Guiñez etal. (1992) used isozymatic variation to studythe genetic structure among 6 localities fromsouthern Perú: Mollendo (17°00’ S), tosouthern Chile: Mehuín (39°27’ S). The authorssuggested the existence of strong geneticstructure and defined three genetic groups: Thefirst represented by specimens from thenorthern localities: Mollendo and Iquique(24º14’ S); the second by specimens fromcentral and northern Chile: Antofagasta (23º41’S) and Coquimbo (32º08’ S), and the third byspecimens form central and southern Chile: ElQuisco (33º24’ S) and Valdivia (39º27’ S). Incontrast, Gallardo & Carrasco (1996) using thesame genetic markers analyzed C. concholepaspopulations from localities in central Chile:Quintay (33°10’ S), to southern Chile: ChiloéIsland (42°38’ S), and showed low levels ofpopulation subdivision and suggested theexistence of genetic cohesiveness among C.concholepas.

An evaluation of the present taxonomywithin the genus Concholepas is difficult sinceall the species, with the exception of C.concholepas, are extinct. Therefore, amolecular approach is impracticable.Nevertheless, the comparison of shell traits andmolecular markers in extant populations maybe useful to determinate the robustness of themorphological traits as an adequate tool toanalyze the taxonomy of the genus. Also thismay be useful to explore if extant populationsof C. concholepas constitute a single taxonomicunit along its present distributional range. Thisis considered as a key issue linked to themanagement and conservation of the species.Therefore, in this paper we first attempt acomprehensive review on the taxonomy,historical relationships and geographicaldistribution of Concholepas species, so tocontribute towards the reconstruction of the


past history of the genus. Second, we discussthe robustness of using shell traits whenclassifying specimens of the genusConcholepas by comparing variations oflength/width ratio and genetic diversity indexesbased on sequences of mitochondrial DNA(mtDNA) in spatially distant localit iesinhabited by C. concholepas. Third, using amolecular approach, we evaluate the taxonomicstatus of C. concholepas along its presentgeographical range, including samples fromPerú, continental Chile and the Juan FernándezArchipelago.

MATERIAL AND METHODS

Bibliographic review of the taxonomy andpaleobiogeography of Concholepas

To understand the evolutionary history ofthe genus Concholepas, published articles onthe taxonomy and geographical distribution ofthe genus were reviewed. Two methods wereused to obtain information: (a) we followed thereview made by Castil la (1988), payingparticular attention to publications by Herm(1969), Beu (1970), Vokes (1972), Lambiotte(1975) and Stuardo (1979), (b) conducted asearch in the ISI Web of Science database(1989 to 2006), finding 60 publications notincluded in Castilla (1988). Then, we selectedthose papers that included in their abstracts thewords: fossil record, evolution,paleogeographical distribution andConcholepas.

Sample collection of extant C. concholepas

The geographical distribution of C.concholepas covers more than 7,000 km alongthe Southeastern Pacific coast, from 6° S inPeru to 56° S, in the tip of Chile. Thus, to havea representative sampling, we collected adultsor juveniles along its distributional range takeninto account the biogeographical subdivision ofthis region proposed by Camus (2001) (Fig. 1).In the Peruvian Province (PP) we collectedspecimens from the subtidal in Matarani(17°00’ S, 72°18’ W, n = 29); in theIntermediate Area (IA) we collected specimensfrom the subtidal in: El Quisco (33°23’ S,71°42’ W, n = 27), and Las Cruces (33°31’ S,

71°38’ W, n =27); in the Magellan Province(MP) we collected specimens from the subtidalat Puerto Aguirre (45°15’ S, 72°40’ W, n = 29).In order to test for potential differences in L/Wratio between Concholepas from intertidal andsubtidal habitats we additionally collectedsamples from the intertidal at El Quisco (n =19) and Las Cruces (n = 27). After collections,two morphometric traits were measured in eachindividual: (1) total length, corresponding tothe antero-posterior length measured from theborder of the siphonal channel to the top of theposterior edge of the aperture, (2) total width,corresponding to the widest part of the shellwhen measured perpendicular to its length.Measurements were taken to the nearest 0.05mm using a digital caliper. Immediately after, apiece of approximately 2 cm3 of tissue was cutfrom the border of the foot muscle and storedin 95 % ethanol to the posterior DNAextraction. Additionally we collected foottissue samples of C. concholepas specimensfrom Juan Fernández Archipelago (Punta TresReyes, 33º37’ S -78º52’ W); however the shellswere not accessible for morphometric analysis.

Variation length/width ratio

We selected the length/width ratio (L/W) as acritical Concholepas morphological trait givenits common use in taxonomic studies (Herm1969, Stuardo 1979, DeVries 1995, DeVries2000). The L/W ratio was calculated using twomorphometric traits, total length and totalwidth, as used in previous works (Stuardo1979, DeVries 1995). To test for differences inL/W ratio among localit ies along thegeographical range of distribution of C.concholepas we made a comparison using onlysubtidal specimens (Table 2). In order to testfor potential differences in L/W ratio insubtidal and intertidal environments, we usedspecimens collected at both habitats in LasCruces and El Quisco. We estimated the L/Wratio expressed as the mean value and standarddeviations per locality. Differences in L/Wratio among populations were evaluated usingANOVA analysis considering the L/W ratio asthe dependent variable and locality as thegrouping variable. To test for potentialdifferences in L/W ratio between subtidal andintertidal habitats we performed ANOVA andTukey HSD test (Sokal & Rohlf 1981), letting


L/W ratio as dependent variable and localityand habitat as grouping variable.

Genetic analysis

We used the cytochrome oxidase Imitochondrial gene (COI) because is widelyused in marine species and universal primerswere developed by Folmer et al. (1994). Totalgenomic DNA was extracted from muscletissue using a standard phenol/chloroformprotocol. The amplifications were performed asdescribe by Jolly et al. (2006). Double strandedPCR products were sequenced for eachindividual using an ABI PRISM® 3100automated DNA Sequencer (Perkin-ElmerApplied Biosystems, Foster City, California,USA). Sequences were edited and aligned usingProSeq v 2.9 (Filatov 2002) and finalalignments were adjusted by eye. Weperformed a test introduced by Xia et al. (2003)to measure substitution saturation in a set of

aligned nucleotide sequences, to evaluatewhether these sequences are useful forphylogenetic analyses.

To best represent the phylogeneticrelationships within C. concholepas , amaximum likelihood (ML) phylogeneticapproach reconstruction based in the bestsubstitution evolutionary model for the COIhaplotypes was constructed. The simplest MLmodel that best explained the data wereestimated using the Akaike InformationCriterion (AIC) in the program MODELTEST3.0 (Posada & Crandall 1998). Additionally,bootstrap resampling (Felsenstein 1985) wasapplied to assess support for individual nodesusing 1,000 bootstrap replicates. The gastropodThais (Stramonita) chocolata (Duclos 1832),another Rapaninae endemic of the SoutheasternPacific was used as outgroup. Thereconstruction of phylogenetic trees wasperformed using PAUP* software (Swofford2002).

Fig. 1: Map depicting the samples localities (A) and the geographic range distribution of fossilspecies of the genus Concholepas (B). In (A), PP corresponds to the Peruvian Province, IA corres-ponds to the Intermediate Area (IA) and MP is Magallanic Province. Species in (B) are marked bynumbers that correspond to table 1.Mapa mostrando la ubicación geográfica de las localidades muestreadas (A) y el rango geográfico de las especies fósilesdel género Concholepas (B). En (A), PP es la Provincia Peruana, IA corresponde el Área Intermedia y MP representa laProvincia Magallánica. Las especies en (B) están marcadas con números que se corresponden con los de la Tabla 1.


To analyze the genetic composition in C.concholepas we compared the genetic diversityamong localities. The standard genetic diversityindices, such as the number of haplotypes (nH),number of segregating sites (S), haplotypediversity (He), the nucleotide diversity (π) andthe pairwise differences between sequences (Π)for each locality were estimated using Arlequinversion 3.01 (Excoffier et al . 2005).Additionally, we construct a matrix of pairwisegenetic differences among localities (Pairwiseθ, Weir & Cockerham 1984). The significanceof the pairwise θ values was tested bypermutation.

RESULTS

Taxonomy and paleobiogeography ofConcholepas

Since the taxonomic classification inside theConcholepas clade has been recently changed(DeVries 1995, 2000, Vermeij 1998), thegeographical distribution of the genusConcholepas has suffered differentinterpretations according to different authors.Two main clusters may be considered in thehistory of this genus: a non-South Americanand a South American (Herm 1969, Beu 1970,Vokes 1972, Lambiotte 1975, Stuardo 1979,Kensley 1985). The non-South American cladeshows a disjoint distribution (Fig. 1). However,on the basis of morphologic traits the non-South American species were assigned to thegenus Concholepas (Herm 1969, Beu 1970,Vokes 1972, Lambiotte 1975, Stuardo 1979).All non-South American fossil species arerestricted to Miocene strata. The oldestreported species of the genus is Concholepasdrezi (Vokes, 1972), which dates from the lateearly Miocene, of the Chipola Formation inFlorida, USA (Fig. 1). From the MiddleMiocene, two species have been reported,Concholepas deshayesi (Rambur, 1862) fromTouraine, France, and Concholepas antiquata(Tate, 1894) from Port Philip Bay and MuddyCreek, Hamilton, Australia. Finally,Concholepas pehuensis (Marwick, 1926)occurred in the late Miocene of North Taranaki,New Zealand. In addition, based on the stratatype occurrence and related fauna, all Miocenespecies of Concholepas were associated with

warmer and deeper marine environments thanthose experienced by modern C. concholepas.Moreover, Beu (1970) and Vokes (1972)suggested that the thin shell character in thisnon-South American clade is a signature thatolder species of the genus lived inenvironments of low wave energy; suggestingthat the genus Concholepas invaded the rockyintertidal environments following the Mioceneepoch. DeVries (1995), compared the speciesassigned to Concholepas and suggested thatnon-South American and South Americanspecies of Concholepas were two different andnon related taxa. Vermeij (1998) re-evaluatedthe taxonomic position of non-South AmericanConcholepas species, and assigned all non-South American species to the genus Edithaisand designated C. drezi as the type species(Table 1). According to Vermeij (1998), thekey morphological differences between bothgenera are: (1) Concholepas species exhibitshells with a high L/W ratio, whereas inEdithais the width exceeds the length, (2) inshells of Edithais, the spire (the posterior endof the outer lip) extends beyond the apex;while, in contrast in Concholepas, the spireextends above the adapical end of the aperture,(3) the spiral cords in Concholepas are stronglyornamented with scales and nodes, whereasthose of Edithais are finer and lack axialornaments. However, in the Vermeij & Carlson(2000) analysis of the subspecies Rapaninae,Concholepas and Edithais appears as sistergenera located at the base of the phylogenetictree, where the phylogeny was unresolved andhas low statistic support.

The South American Concholepas clade hasundergone taxonomical re-arrangements andnew fossil species have been described. Atpresent the genus Concholepas is composed bysix species, out of which C. concholepas is theonly extant species (Fig. 2). The older fossilrecords of the species, that represents theancestral species of Concholepas in SouthAmerica, was found in Lomitas, Pisco basin(Perú), corresponding to Concholepas ungis(DeVries 1995). This species inhabited themarine realm of the early to middle Miocene(about 20.5 million years before present) and hasbeen found only in south-central Perú (DeVries1995). Concholepas ungis has a small shell size(not exceeding 30 mm in length) compared withother members of the genus. However, DeVries


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(1995) sustained that the uniformly convex bodywhorl, the long and broad aperture and thestrong fasciolar ridge of this species representkey characters for the inclusion of this speciesinto the genus Concholepas. Later DeVries(2000) described Concholepas chirotensis(DeVries 2000), from the end of the middleMiocene (16.4-11.2 million years beforepresent) at Quebrada Chiroteo, in southern Perú.Apparently, these two Miocenic species werenot contemporary, and both are found indepositional environments characteristic of inner

shelf and shallow subtidal systems suggestingthat these taxa inhabited sandy bottomenvironments characterized by low wave energy(DeVries 1995, 2000).

From the Pliocene epoch two fossil speciesare recognized: Concholepas kieneri (Hupé,1854) and Concholepas nodosa (Möricke, 1896).These species were recognized early from thelate Pliocene fossil deposit in the CoquimboFormation, northern Chile (Herm 1969, Beu1970, Vokes 1972). However, DeVries (1995)described new reports broadening the

Fig. 2: Evolutionary hypotheses of Concholepas (Lamarck, 1891) in South America. The Cruz inSouth Africa has been referenced to the fossil record of the extant C. concholepas (see text).Pictures of fossil species were obtained from Tom DeVries collection: C. unguis USNM 447096(holotype); C. chirotensis: USNM 447121 (paratype); C. nodosa USNM 447122; C. kieneri USNM447088 and C. camerata USNM 447129 (holotype). Numbers in superior boxes correspond tofollow references: (1) Zachos et al (2001); (2) Lawver & Gahagan (2003); (3) Martinez-Pardo(1990); (4) Tsuchi (2002); (5) Zinmeister (1978); (6) OPD partnership (2002); (7) Clapperton(1994); (8) Rivadeneira (2005); (9) Moy et al. (2002); (10) Loubere et al. (2003).Hipótesis de la evolución del género Concholepas (Lamarck, 1891) en Sudamérica. La cruz en el sur de África hacereferencia al registro fósil del C. concholepas en esa área (ver texto para detalles). Fotos de las especies fósiles fueronobtenidas desde la colección del Dr. Tom DeVries: C. unguis USNM 447096 (holotype); C. chirotensis: USNM 447121(paratype); C. nodosa USNM 447122; C. kieneri USNM 447088 and C. camerata USNM 447129 (holotype). Los númerosen la parte superior corresponden a las siguientes referencias: (1) Zachos et al (2001); (2) Lawver & Gahagan (2003); (3)Martinez-Pardo (1990); (4) Tsuchi (2002); (5) Zinmeister (1978); (6) OPD partnership (2002); (7) Clapperton (1994); (8)Rivadeneira (2005); (9) Moy et al. (2002); (10) Loubere et al. (2003).


geographical distribution of both species furthernorth into south-central Peru, up to 14º46’ S.These reports have also extended the temporalrange of these species: C. kieneri ranging fromthe upper late Miocene to Pliocene (11.2-1.8million years before present) and C. nodosafrom the early Pliocene to late Pliocene (5.3-1.8million years before present). Lately, DeVries(2000) introduced Concholepas camerata(DeVries, 2000), a species of short durationduring the late Pliocene (3.6-1.8 million yearsbefore present), from the Sacaco Basin (at 14º S)in southern Perú.

Regarding the extant species of the genus,the first fossil record of Concholepasconcholepas was reported in late Pleistocenemarine terrace deposits from northern Chile(Herm 1969, Stuardo 1979, Guzmán et al.20001). However, DeVries (1995) expanded thespatial and temporal distribution of the fossilrecord reporting the species from the latePliocene to middle Pleistocene (ca 3.6-1.0million years before present) in outcrops fromthe Talara Basin (4º15’ S, northernmost Perú).An outstanding paleobiogeographic feature ofC. concholepas is its disjunctive distribution. Infact, Kensley (1985) recorded the species inlate Pleistocene coastal deposits from westSouth Africa-Namibia (about 26° S). Accordingto this author, the South African C.concholepas fossils are indistinguishable fromthose in South America. Castilla & Guiñez(2000) agreed with Kensley (1985) andsuggested that the South Africa fossil shells donot differ from the approximately 8.000-9.000years archeological shell excavated C.concholepas from central Chile (Jerardino et al.1992; in 1999, J. C. Castilla analyzed shells ofS. African Concholepas fossils in the CapeTown Museum of Natural History).

Variation length/width ratio on extant C.concholepas

The mean L/W ratio for the whole data set (n =158, not including Juan Fernández Archipelagosamples) was 1.35 ± 0.1 (minimum: 1.06,maximum: 1.71). Figure 3 shows the mean L/W

ratio by locality. The mean L/W ratio wassignificantly different among localit iesdistributed along the geographical rangedistribution of C. concholepas (F = 14.33, P =0.000). For subtidal samples (n = 112specimens) the mean of L/W ratio was 1.31 (±0.07), (maximum= 1.35 in Puerto Aguirre andminimum= 1.25 in Las Cruces, see details inTable 2). For the intertidal samples (n = 46specimens) the mean L/W ratio was 1.39 (±0.11) (maximum = 1.47 in Las Cruces andminimum = 1.36 in El Quisco, see details inTable 2). The comparison of L/W ratio betweenspecimens from intertidal and subtidalenvironments, from Las Cruces and El Quisco,showed that there is a significant effect ofhabitat factor (F = 95.8, P = 0.000) and theinteraction term habitat*locality” (F = 58.34, P= 0.000) but no for locality alone (F = 1.28, P =0.26). A Tukey HSD test showed that samplesfrom Las Cruces intertidal are significantlyhigher from the other samples sites.

Genetic analysis

In total we obtained a fragment of 658 basepairs of the mitochondrial gene COI, from 179individuals of C. concholepas. A total of 103polymorphic sites and 80 haplotypes wereidentified. The GenBank accession numbersfor these haplotypes corresponds fromEU250850 to EU250929. The substitutionsaturat ion test demonstrated that oursequences have little saturation (Iss = 0.017 <Iss c = 0.719, df = 341, P < 0.0001), thusvalidating their use for phylogenetic inference.Results of the ModelTest showed that the mostdescriptive model of evolution for COI genewas K81uf+I+G (K81 is a model with unequalbase frequencies , Kimura 1981) with aproportion of invariable sites (I = 0.48) andgamma distribution (gamma shape = 1.31).Few branches were supported by bootstrapvalues greater than 50 % (Fig. 4) and the MLnucleotide distance among haplotypes variedbetween 0.15 to 1.2 % (data non show). Thereis not a clear pattern for cluster compositionof the haplotypes. In fact, all the haplotypeswere distributed along the tree independentlyof the sampled localities. Thus, the COImtDNA tree reconstruction suggests theexistence of only one phylogenetic clade in C.concholepas.

1 GUZMán N, C Marquardt, L Ortlieb & D Frassinetti(2000) La malacofauna neógena y cuaternaria del áreade Caldera (27-28° S): especies y rangosbioestratigráficos. Actas of the Congreso GeológicoChileno 9: 476-481.


Fig.3: L/W ratio by localities and average of subtidal ad intertidal habitats.Razón L/W por localidades y promedio de hábitat submareal e intermareal.

TABLE 2

Sampled localities of Concholepas concholepas. Mean L/W ratio, Number of samples (n), numberof polymorphic sites (S) and number of haplotypes (nH) per locality are showed. The genotypic

diversity (He), nucleotide diversity (π) and Mean number of pairwise differences betweensequences (Π) were calculated using Arlequin software. Standard deviations are showed in

parenthesis

Localidades muestreadas para C. concholepas. La media de la razón L/W, el número de muestras por sitio (n), el númerode sitios polimórficos (S), y el número de haplotípos por localidad (nH) son mostrados. La diversidad genética (He), la

diversidad nucleotídica (π) y el número promedio entre pares de secuencias (P) fueron calculados usando Arlequín.Desviaciones estándar son mostradas en paréntesis

Habitat Locality L/W Ratio (± SD) n S nH He (± SD) π (± SD) Π (± SD)

Intertidal Las Cruces 1.47(± 0.13) 27 32 22 0.96 (± 0.03) 0.004 (± 0.002) 2.64 (± 1.45)

El Quisco 1.36 (± 0.08) 19 15 11 0.83 (± 0.09) 0.003 (± 0.002) 1.77 (± 1.07)

Total 1.39 (±0.11) 46 42 35 0.91 (± 0.04) 0.004 (± 0.002) 2.20 (±1.26)

Subtidal Las Cruces 1.25 (± 006) 27 33 23 0.94 (± 0.04) 0.005 (± 0.003) 3.19 (± 1.70)

El Quisco 1.33 (± 0.05) 27 24 14 0.80 (± 0.08) 0.003 (± 0.002) 2.03 (± 1.18)

Matarani 1.31 (± 0.06) 29 22 18 0.86 (± 0.06) 0.003 (±0.002) 2.01 (± 1.16)

Puerto Aguirre 1.35 (± 0.10) 29 25 19 0.86 (±0.06) 0.003 (± 0.002) 2.23 (± 1.27)

Juan Fernández n.i. 21 20 16 0.97 (±0.02) 0.04 (±0.003) 2.99 (±1.62)

Total 1.30 (±0.05) 133 85 80 0.89 (± 0.04) 0.004 (± 0.002) 2.49 (±1.38)

n.i.; no information


The genetic analyses inside the cladeshowed a general pattern of high level ofpolymorphism and low genetic structure in thesampled local i t ies . For example, thecomparison among localities showed highlevel of genetic polymorphism (Table 2).While, the nucleotide diversity was low andthe mean number of pairwise differencesbetween sequences ranged from 1.77 inQuisco subtidal to 2.99 in Juan Fernandezsamples (Table 2).

The subtidal and intertidal habitats werecompared using samples from Las Cruces and

El Quisco. No differences in gene andnucleotide diversity between subtidal andintertidal samples were found (Student t-tests; P = 0.88 and P = 0.55). Low pairwiseθst values were found among all sampledlocalities. Only 3 of 21 comparisons resulteds igni f icant a t 5 % level . Here , JuanFernandez Archipelago appears to begenet ica l ly d i f ferent f rom Las Crucesintertidal, Quisco Intertidal and Matarani(Table 3). However, non-significant φstpairwise comparisons were detected afterBonferroni correction (Table 3).

Fig.4: Maximum Likelihood tree among the COI haplotypes of Concholepas concholepas; (A)phylogram, and (B) subtree showing the relations inside the in-group. Values above each branchindicate the bootstrap percentages (> 50 %, 1,000 replicates) for the ML analysis.Árbol de Máxima Verosimilitud entre los haplotipos del gen COI en C. concholepas; (A) filograma y (B) subárbolmostrado las relaciones dentro del grupo. Valores sobre ramas indican el porcentaje de “bootstrap” (> 50 %, 1.000réplicas).

(B)(A)


DISCUSSION

Taxonomy and paleobiogeography of Concho-lepas

Based on this literature review, we postulatedthat the evolutionary pattern in Concholepasappears to represent a chronospecies (Fig. 2),receiving different names for the successivephenotypically forms, and where the fossilsspecies appear to be distinguishable statesalong the evolving lineage (Stanley 1978).Therefore, we postulated that the termmorphospecies may be more appropriate torefer to the fossil species of the generaConcholepas. Evidences to support the abovestatements are: (1) the endemic character of thegenus, which has been present only in thesoutheastern Pacific coast. Deposits from theNavidad Formation (32°30’- 34°00’ S), one ofthe most extensively studied onshore unit inChile and considered as a reference for themarine Neogene of the Chilean coast(Frassinetti & Covacevich 1981, 1982, DeVries& Frassinetti 2003, Groves & Nielsen 2003,Nielsen 2004, 2005) has not yield specimens ofthe genus Concholepas. Therefore, only themost recent species, C. concholepas, appears tohave a wide extension along the SoutheasternPacific coast. (2) During its evolutionaryhistory the genus Concholepas gradually

changed from shallow subtidal environments tomore exposed wave energy ones (i.e., rockyintertidal). The fossil records show that alongthese transitions (Fig. 2), a series ofmorphospecies occurred sequentially. Duringthe Pliocene epoch there were two coexistingspecies: C. kieneri and C. nodosa, which maybe considered as a single radiation event in thisgenus. (3) Lastly, transitional states ofmorphologically different lineages in the genushave been recently identified: C. chirotensisand C. camerata. Both species appear to havehad short lived period (DeVries 2000) and wereextant during the transition of Miocene-Pliocene and Pliocene-Pleistocene,respectively.

Following these perspectives, the evolutionof Concholepas apparently responded toenvironmental changes that occurred in thesoutheastern Pacific coast associated with theconsolidation of the upwelling-Humboldtcurrent system. The first change inConcholepas lineage may have occurred duringthe late Middle Miocene (about 15-12 millionyears before present), associated to a coolingperiod due to the gradual decline of surfaceseawater temperature and upwelling activationin the Peruvian coast (Ibaraki 1997). Accordingto the fossil record, Concholepas ungis wasthen extinct, while Concholepas chirotensisappeared around the late Middle Miocene

TABLE 3

Pairwise φst comparison between C. concholepas localities (below diagonal); (*) significant Pvalues at α = 0.05 (above diagonal). Only non significant values were obtained after Bonferroni

correction for multiple tests

Comparación de φst entre pares de localidades muestreadas (bajo de la diagonal); (*) valores de probabilidad significativosa α = 0,05 (sobre la diagonal). No se encontraron valores significativos de diferenciación después de una corrección de

Bonferroni para pruebas múltiples

1 2 3 4 5 6 7

1. Matarani - 0.431 0.092 0.105 0.039* 0.350 0.378

2. Quisco subtidal -0.0001 - 0.321 0.441 0.076 0.686 0.698

3. Las Cruces subtidal 0.0084 0.0034 - 0.342 0.056 0.477 0.569

4. Puerto Aguirre 0.0092 0.0005 0.0019 - 0.102 0.518 0.626

5. Juan Fernández 0.0201 0.0165 0.0173 0.0140 - 0.042* 0.026*

6. Quisco intertidal 0.0025 -0.0047 -0.0006 -0.0020 0.02791 - 0.883

7. Las Cruces intertidal 0.0004 -0.0024 -0.0004 -0.0023 0.0221 -0.0071 -


(DeVries 2000). However, this morphospeciesappears to have had a short-lived period andwas limited to southern Perú (fossils have beenregistered around 16º S). In fact, in accordancewith DeVries (2000), there is a gap in thetransition from C. chirotensis to C. kieneri andtheir phylogenetic relationship remains unclear(Fig. 2). From Miocene to Pliocene, the genusConcholepas began to expand southward:Concholepas kieneri and in upper LateMiocene inhabited the coast of southern Perú.During the Pliocene (3.6-1.8 million yearsbefore present), C. kieneri reached the northerncoast of Chile, following the evolution of theoceanographic system along the southeasternPacific (Jacobs 2004). During the Pliocene, theclosing of the Panama seaway, as well as theconsolidation of the modern Humboldt Currentsystem and the expansion of coastal upwellingin the Pacific, took place (Zinmeister 1978,Ortlieb 1995, Villagrán 1995, Ibaraki 1997,Zachos et al. 2001, Nishimura 2002, Tsuchi2002). During the Pliocene epoch two speciesof Concholepas co-occurred along thesoutheastern Pacific coast (Fig. 2). The macro-environmental variations may have increasedthe diversity of coastal environmentalconditions and caused an upsurge in themollusk speciation processes. For instance,forcing the most primitive Concholepas forms(C. kieneri) to split into two branches, and oneof them may have derived into themorphospecies Concholepas nodosa (Fig. 2);while the other remained unchanged. Duringthis epoch, C. kieneri and C. nodosa appearedin the fossil record as sympatric species with asimilar geographical distribution from southernPerú to northern Chile; and, as suggested by thefossil record during this period, the genus mayhave expanded to more exposed coastalhabitats.

The transition from the Pliocene to thePleistocene was marked by mass extinction ofmollusks in the Peruvian and northern Chilecoasts (Herm 1969, Vermeij 1987, DeVries2001, Rivadeneira 2005). The development ofhypoxic conditions imposed by a shallowoxygen minimum zone as a consequence of theNeogene onset of coastal upwelling in thePeruvian Province has been hypothesized to bethe responsible mechanism for the Pliocenemollusk mass extinction in this area. The effectof this extinction in the Peruvian and northern

Chile coasts has been recently reviewed for themarine bivalve species (Rivadeneira 2005).This author proposed a model where the onsetof the Humboldt Upwelling System acted as adouble-edge sword, devastating marinediversity on one side and promoting theincrease in abundance of the remaining formson the other. It is likely that these events mayhave promoted the extinction of C. kieneri andC. nodosa. At the same time, Concholepascamerata appeared in southern Perú (about 15°S), representing a short-lived morphospecies.The short history of this morphospecies mayalso be connected with the massive molluskextinctions in the Peruvian Province during thePliocene-Pleistocene boundary, since the fossilrecords show up that 70 % of mollusk thespecies went extinct during these events (Herm1969, DeVries 20012). Thus, during thePleistocene only one species of Concholepas isfound in the fossil record: Concholepasconcholepas.

The existence of African fossils of C.concholepas in the Pleistocene (Kensley 1985)stresses the importance of Concholepasdispersal potential on the evolutionary historyof the species, and may explain the presentwide geographical range extension of thespecies in South America. According toKensley (1985) the African fossils of C.concholepas may represent a founding andpioneer population that settled on the rockyintertidal of South Africa-Namibia, followingdrifting larvae transported via the West WindDrift from southern South America to the west.Castilla & Guiñez (2000) suggested that thefossil record of C. concholepas present inSouth Africa-Namibia, may have originatedfrom juvenile/adult groups of Concholepasarriving to the west African coast onconsolidated drifting substrata, as a case ofkelp-rafting across oceanic routes (e.g., OO’Foighil et al. 1999, Thiel & Haye 2006). Abreeding population of C. concholepas mayhave established in these coasts, but went laterextinct due to either fluctuation in sea level,limited reproductive potential of a small localpopulation, or by the negative consequences of

2 DEVRIES TJ (2001) Contrasting patterns of Plioceneand Pleistocene extinctions of marine mollusks inwestern North and South America. Geological Societyof America, Abstract A-35.


a strong founder effect. The long distancedispersal via rafting has been used to explainthe presence of closed related phylogeneticclade in opposite marine coastal margins. Forexample, the calyptraeid limpet, Bostrycapuluscf. aculenta sp.1 (Collin 2003b), a directdeveloper, inhabits both the east coast of SouthAmerica and South Africa. Molecular data haveshown that the South African population hasrecently derived from the South Americanpopulation, an event that may have occurred bytrans-Atlantic-rafting (Collin 2003b).Moreover, recent phylogeographic studies ofsouthern marine taxa (e.g. , Diloma andParvulastra) imply that passive rafting cannotbe ignored as an important mechanism forlong-distance dispersal (Donald et al. 2005,Waters et al. 2007).

Two ecological aspects of C. concholepascould be the most important elements todetermine its long distance dispersal: (a) thecharacteristics of the planktonic larvae; (b) thetrophic ecology of C. concholepas. Briefly,

C. concholepas is gonochoric but lackssexual dimorphism (Castilla 1983). Females layegg capsules on low intertidal and shallowsubtidal rocky surfaces (Castil la 1979,Manríquez & Castil la 2001). Afterapproximately 1 month of intracapsulardevelopment, small planktotrophic veligerlarvae are released and spend at least 3 monthsin the water column (DiSalvo 1988, but seeMolinet et al. 2005). Once the larvae becomecompetent, they dwell at the sea surface untilthey settle on rocky intertidal and shallowsubtidal habitats (Stotz et al. 1991, Moreno etal. 1993, Martínez & Navarrete 2002). TheConcholepas larval duration in the planktonsuggest a high potential for dispersal. However,Poulin et al. (2002b) reported a verticalmigration mechanism for Concholepas larvaeto avoid their offshore dispersal. On otherhand, C. concholepas is a carnivore, slowmoving muricid, preying predominantly onmussels, barnacles and ascidians (DuBois et al.1980). Additionally, it has been demonstratedthat barnacles induce settlement behavior andmetamorphosis of competent larvae (Manríquezet al. 2004), suggesting that larvae of C.concholepas respond to chemical cuesoriginated from their most preferred prey (Stotzet al. 2003). There are evidences for therecruitment and establishment of juvenile of

Concholepas, mussels, barnacles and ascidiansinside the holdfast of kelps (Cancino &Santelices 1984, Vásquez & Santelices 1984).Thus, newly settled individuals of Concholepasinside these holdfasts could encounter apermanent solid substrate and abundant preyitems (mussels, barnacles, ascidians, etc.). Thusthe rafting by kelps may be a probablymechanism for long distance dispersal in C.concholepas.

Morphologic and genetic diversity in extantpopulations of C. concholepas

The L/W ratio was used to describe the rangeof morphological variation along thegeographical distribution of the extant C.concholepas (more than 7,000 km of coast lineand oceanic islands). Our analysis showed thatthere is much more variation on L/W ratio thanreported by DeVries (1995) and Vermeij (1998)and interestingly, this range of variationincorporates all variation detected in thestudied fossil species. For instance, theminimum value of L/W ratio for C.concholepas detected in our analysis was 1.06,the same value reported for Edithais deshayesiby DeVries (1995) (Table 1). Moreover, in thisregards the literature contains contradictoryinformation. DeVries (1995) reported forPleistocene specimens of C. concholepas anaverage L/W ratio of 1.25 (Table 1), which canbe compared with the mean value of 1.35 ± 0.1for the whole data set reported in our analysis(Table 2). Considering the variation in L/Wratio detected among extant C. concholepas(Fig 3), the usefulness of this character fortaxonomic studies remains ambiguous. In fact,spatial variation in L/W ratio detected here mayreflect phenotypic plasticity associated withhydrodynamics stress or other environmentalcues (e.g., Palmer 1985, 1990, Trussell 1997).For instance, several ecological factors areknown to influence shell shape in mussels(Brown et al. 1976, Richardson & Seed 1990),oysters (Chinzei et al. 1982), clams (Cigarria &Fernández 1998) and tunicates (Paine &Suchanek 1983). Our results confirm that theshell morphology could be highly variable to beused in taxonomic issues, and thedifferentiation in L/W ratio among extant C.concholepas probably corresponds to particulargrowth conditions (differences between


intertidal versus subtidal), or perhaps is due todifferent hydrodynamics patterns along itsrange distribution. This differentiation of L/Wratio has been reported in patellogastropodlimpets and some authors have suggested that iscaused by tidal level, desiccation stress orwater turbulence (Ino 1935, Segal 1956,Vermeij 1973, Simpson 1985). These resultsare in conflict with a previous analysis byStuardo (1979), who gives to this morphologicvariability a taxonomic character. In fact, basedmainly on analysis of these characters, heproposed the existence of a subspecies in theJuan Fernández archipelago: Concholepasconcholepas fernandizianus.

Two important results upsurge from ourgenetic analysis of the COI sequences in C.concholepas. First, the ML tree of the COIhaplotypes of C. concholepas from fivelocalities spatially separated along its rangedistribution, suggests that a single mitochondrialclade is present along the whole southeasternPacific coast (Fig. 4). Second, the low level ofgenetic differentiation among localities does notsupport the existence of the subspecies C.concholepas fernandizianus (Table 3).

A low level of genetic differentiation wasdetected among all sampled sites (nonsignificant pairwise φsT values and nonsignificant differences in gene diversity indices).These results agree with Gallardo & Carrasco(1996), suggesting genetic cohesiveness amonglocalities from the central-south geographicdistributional range of C. concholepas. On theother hand, our study is in disagreement with theconclusions reached by Guiñez et al. (1992),whom postulated the existence of at least twogenetically structured clusters: a northern Chile-Perú and a center-northern Chile cluster.Differences in the molecular markers used byprevious mentioned authors have prevented usthe comparison among our results and theformer ones. Guiñez et al. (1992) and Gallardo& Carrasco (1996) used isozymes and thesemarkers unmask primarily the genetic changes incoding regions that posses altered amino acidsequences; then the effect of selection onisozymes markers cannot be totally discarded. Amechanism of temporal variation in geneticdifferentiation mediated by selection couldexplain the contradictions between Gallardo &Carrasco (1996) and Guiñez et al. (1992). ElNiño event is the most important perturbation

in the northern part of the range distribution ofC. concholepas. Could it be that the populationstructure detected by Guiñez et al. (1992)actually reflected the consequences of thoseevents on the genetic structure of C.concholepas? The strong effect of the El Niñoevents on the genetic structure of the marinespecies has been reported in this area (forexample for the brow algae Lessonianigrescens; Martínez et al. 2003). In our studywe detected no genetic differentiation amongspatially separated localities. For example, inspite that Matarani (in Perú) and PuertoAguirre (south of Chile) are separated by morethan 3,000 km, the genetic divergence betweenthose populations was only 0.9 % (Table 3).This pattern has been reported in other marinespecies (Uthicke & Benzie 2003, Cassone &Boulding 2006, Zane et al. 2006). Two geneticpatterns could explain the reported apparenthomogeneity in the sampled localities of C.concholepas: (a) broad scale homogeneity, (b)chaotic genetic patchiness (Hellberg et al.2002). The broad scale homogeneity is apattern likely due to high levels of gene flow,which is typically found in marine species withplanktotrophic larvae. On the other hand, ifadults’ populations of a marine species showlow levels of genetic subdivision and ifrepeated sampling of recruits from the samelocality over time reveals a high geneticdifferentiation among different cohorts, onewould expect a chaotic genetic patchinesspattern. In C. concholepas, as in other marinegastropods, random recruitments could favorthe broad genetic homogeneity pattern(Hellberg et al. 2002). However, reproductivesuccess has been shown to vary considerablyamong individuals of marine benthicinvertebrates showing planktonic larval phase(Grange 2005). Thus, only a small portion ofthe individuals may contribute to the nextgeneration, a process resulting into importanttemporal genetic changes, known as the“sweepstake hypothesis” (Hedgecock 1994).Thus, the sweepstake hypothesis may be behindthe present genetic homogeneity observed inthe localities where Concholepas was sampledand consequently a future temporal study of thegenetic variability may be an important nextstep to determine the role of the temporalenvironmental changes and their effect in thegenetic structure of C. concholepas.


Non-significant genetic differentiation wasdetected among continental samples of C.concholepas and the subspecies C. concholepasfernandizianus. The genetic divergence fromthe φsT comparison (Table 3) among thesubspecies of Juan Fernández archipelago andthe continental samples of C. concholepas wasestimated at ca. 1 %, and it does not differ fromthe divergences detected among continentalsampled localities of C. concholepas. Theseresults suggest a recent arrival of C.concholepas to the Juan FernándezArchipelago. However, the present level ofconnectivity among insular and continentalpopulations of C. concholepas is unknown.Based on high degree of endemism in JuanFernández, authors have suggested theexistence of limited species exchange acrossthe northward flow of the Chile-Perú currentsystem (Andrade 1985, Pequeño & Saez 2000).Nevertheless, it has also been suggested theexistence of other mechanisms for biologicalarrivals to the archipelago form the continent;for instance, via the rock lobster fishing boatsmoving between the archipelago and thecontinent, or even the transport of specimensvia air planes, or alternatively due to ENSOevents of such intensity so as to reach thearchipelago (e.g., Silva & Sievers 1973, Arana1987). Further studies are needed to evaluate ifa contemporary connection between JuanFernández archipelago and continentalpopulations of C. concholepas exists, and ifthis has occurred due to Concholepas highlarval dispersal, rafting drift and/ or oceaniccurrents, or if it has happened mediated byaccidental or on purpose human transport.

The studies on causal factors of the presentbiogeography pattern of marine invertebratealong the southeastern Pacific coast are justbeginning. One important component of thesestudies, is to learn about the past history of thespecies, which it will probably related tohistorical process modulating the present levelof biodiversity either between or withinspecies. The evolutionary history ofConcholepas genus could be characterized as aunique evolutionary lineage whichcontinuously was modifying its morphology,evolved to new environments and recentlyreached a wide distribution along of theSoutheastern Pacific coast coast. Moreover, theonly extant species of the genus corresponds to

a single taxonomic unit including JuanFernández Archipelago populations. Fewstudies have compared different localities alongthe distributional range of C. concholepas.Finally, further studies are necessary to clarifythe current level of connectivity amongConcholepas concholepas populations, thepresent level of diversification amongcontinental and insular C. concholepaspopulations and the possible impact of fisheriesin the genetic diversity of the natural andoverexploited populations of C. concholepas.

ACKNOWLEDGMENTS

We are very grateful to Elie Poulin(Universidad de Chile) Alejandro Perez(Oceana Foundation) and Patricio Manriquez(Universidad Austral de Chile) for providingtissue samples of C. concholepas from JuanFernández Archipelago. We also sincerelythank Dr. Tom DeVries, who generouslyprovided photographs of Concholepas fossilspecies and for insightful comments andsuggestions to improve the manuscript. Thisstudy was funded by grants awarded by ECOSN° C03B04 and FONDAP-FONDECYT 1501-0001 Program 6 to the CASEB. L. Cárdenasacknowledges a doctoral fellowship fromCONICYT-Chile and a grant from CNRS andUPMC for travel and stay in France as part ofher co-supervised doctoral thesis. This work ispart of the “Program 1: Biogeography:transition zones and range limits” of LIADIAMS.

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Associate Editor: Elie PoulinReceived June 5, 2007; accepted January 29, 2008

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